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Streptomyces Sp. Strain MUSC 125 from Mangrove Soil in Malaysia with Anti-MRSA, Anti-Biofilm and Antioxidant Activities

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Streptomyces Sp. Strain MUSC 125 from Mangrove Soil in Malaysia with Anti-MRSA, Anti-Biofilm and Antioxidant Activities molecules Article Streptomyces sp. Strain MUSC 125 from Mangrove Soil in Malaysia with Anti-MRSA, Anti-Biofilm and Antioxidant Activities Hefa Mangzira Kemung 1,2 , Loh Teng-Hern Tan 2 , Kok-Gan Chan 3,4,* , Hooi-Leng Ser 2, Jodi Woan-Fei Law 2, Learn-Han Lee 2,* and Bey-Hing Goh 1,5,6,* 1 Biofunctional Molecule Exploratory Research Group (BMEX), School of Pharmacy, Monash University Malaysia, Bandar Sunway 47500, Selangor Darul Ehsan, Malaysia; [email protected] 2 Novel Bacteria and Drug Discovery Research Group (NBDD), Microbiome and Bioresource Research Strength (MBRS), Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia, Bandar Sunway 47500, Selangor Darul Ehsan, Malaysia; [email protected] (L.T.-H.T.); [email protected] (H.-L.S.); [email protected] (J.W.-F.L.) 3 Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur 50603, Malaysia 4 International Genome Centre, Jiangsu University, Zhenjiang 212013, China 5 College of Pharmaceutical Sciences, Zhejiang University, Hangzhou 310058, China 6 Health and Well-Being Cluster, Global Asia in the 21st Century (GA21) Platform, Monash University Malaysia, Bandar Sunway 47500, Subang Jaya, Malaysia * Correspondence: [email protected] (K.-G.C.); [email protected] (L.-H.L.); [email protected] (B.-H.G.); Tel.: +603-5514-5887 (B.-H.G.); Fax: +603-5514-6323 (B.-H.G.) Academic Editors: Maurizio Battino, Jesus Simal-Gandara and Esra Capanoglu Received: 13 June 2020; Accepted: 24 July 2020; Published: 3 August 2020 Abstract: There is an urgent need to search for new antibiotics to counter the growing number of antibiotic-resistant bacterial strains, one of which is methicillin-resistant Staphylococcus aureus (MRSA). Herein, we report a Streptomyces sp. strain MUSC 125 from mangrove soil in Malaysia which was identified using 16S rRNA phylogenetic and phenotypic analysis. The methanolic extract of strain MUSC 125 showed anti-MRSA, anti-biofilm and antioxidant activities. Strain MUSC 125 was further screened for the presence of secondary metabolite biosynthetic genes. Our results indicated that both polyketide synthase (pks) gene clusters, pksI and pksII, were detected in strain MUSC 125 by PCR amplification. In addition, gas chromatography-mass spectroscopy (GC-MS) detected the presence of different chemicals in the methanolic extract. Based on the GC-MS analysis, eight known compounds were detected suggesting their contribution towards the anti-MRSA and anti-biofilm activities observed. Overall, the study bolsters the potential of strain MUSC 125 as a promising source of anti-MRSA and antibiofilm compounds and warrants further investigation. Keywords: Streptomyces; mangrove; anti-MRSA; anti-biofilm; antioxidant; GC-MS; PKS 1. Introduction The emergence of antibiotic-resistant bacteria poses a serious global health problem in which antibiotic-susceptible pathogenic bacteria mount defensive mechanisms against effects of current antibiotics [1]. It is worrisome, as these antibiotic-resistant bacteria have also been identified in food sources [2]. Methicillin-resistant Staphylococcus aureus (MRSA) is a strain of the Gram-positive bacteria Staphylococcus aureus that has acquired resistance towards methicillin, just one year after its introduction in 1960 [3]. Over the years, MRSA has grown resistant to other classes of antibiotics [4]. To date, MRSA constitutes one of the major impediment to treatment strategies of infectious diseases, Molecules 2020, 25, 3545; doi:10.3390/molecules25153545 www.mdpi.com/journal/molecules Molecules 2020, 25, 3545 2 of 20 particularly in hospital settings, affecting mostly immunocompromised patients [5] with a high prevalence of MRSA (<50%) reported in the United States, South America and Asia [6]. It has been known that MRSA cause severe complications, such as pneumonia and even sepsis, in which if not treated immediately, can progress on to death. The persistence and spread of MRSA in hospital settings is of great concern, as MRSA has been shown to produce protective biofilm layers [7] rendering antibiotics less effective in eradicating them. In spite of efforts to introduce several new anti-MRSA drugs, which are derivatives of traditional antibiotics [6], vancomycin and daptomycin remain superior in treating complicated MRSA infection [8]. Yet, few studies from clinical settings reported findings of MRSA from patients treated with vancomycin [9] and daptomycin [10]. The limited treatment options at hand coupled with the growing resistance to the last resort first-line anti-MRSA drugs has urged the World Health Organization in early 2017 to consider MRSA in the list of antibiotic-resistant bacteria for new drug development [11]. The Gram-positive bacteria Streptomyces is a genus belongs to Actinobacteria phylum and exhibits mycelial growth characteristics [12]. The genus Streptomyces continues to be an important microbe for research as evidenced having the largest number of validly published species with 874 species recorded in the database of List of Prokaryotic names with Standing in Nomenclature (LPSN) [13] at the time of writing (24/4/2020). Moreover, it remains the most sought after microbe for production of biologically active metabolites [14,15]. Many of the antibiotics routinely used for treating infections caused by bacteria have been naturally recovered from Streptomyces [16] including the anti-MRSA drugs vancomycin and daptomycin that are used to treat severe infections associated with MRSA. According to a review by Kemung, et al. [17], Streptomyces have proven to be a great source of anti-MRSA and anti-biofilm compounds. In fact, more than 124 compounds showing anti-MRSA activity have been previously reported from Streptomyces. They remain to date, a valuable resource of new drugs with renewed interest in Streptomyces from mangrove forest ecosystems [18]. Mangrove forests are an unique ecosystem situated between the coastal margins and marine ecosystems and are located in 118 coastal and sub-tropical countries [19]. Given their unique geographical location, mangrove forests and other living organisms, therein, have adapted to grow exclusively in warm tropical and subtropical climates (>24 ◦C) [20] while constantly exposed to the harsh saline ocean waters as well as changing tides and acidic soil [21]. These circumstances are driving the living organisms thriving in mangrove ecosystem to evolve and to withstand these harsh environmental conditions. Hence, mangrove ecosystems are regarded as a “productive” ecosystem whereby the residing microorganisms develop physiological functions that enable the production of enzymes and molecules to cope with the harsh conditions [22]. A rich biodiversity translates to a rich chemical diversity, and this is evidenced in that various resources are derived from mangroves and utilized in traditional medicines [23]. The microbiological diversity in the mangrove soil, particularly the Streptomyces, and their biosynthetic potentials remain underexplored [24]. Many of the lead compounds reported from mangrove forests were isolated from endophytic fungi with few reported from Streptomyces [25]. Streptomyces are aerobic saprophytes and feed on dead and decaying materials [12] by the production of various extracellular enzymes [26]. Although Streptomyces are predominantly aerobic bacteria, they thrive in an anoxic mangrove soil environment where they are constantly exposed to oxidative stress. It is not surprising to find Streptomyces from stressful ecosystem such as mangrove forest, produces secondary metabolites to assist in the defence mechanisms, particularly antioxidants are used to prevent oxidative damage. The antioxidant potential of several mangrove Streptomyces in Malaysia have been reported [27–29]. To date, the mangrove forest remains largely an understudied ecosystem with respect to investigating their secondary metabolites which are valuable sources for future development of therapeutics [24]. The aim of the current study was to evaluate the anti-MRSA, anti-adherence and antioxidant potentials of a mangrove-derived Streptomyces sp. strain MUSC 125. The study revealed that strain MUSC 125 methanolic extract exhibited anti-MRSA, anti-adherence property towards the MRSA biofilm formation and antioxidant activity. The gas chromatography-mass Molecules 2020, 25, 3545 3 of 20 spectroscopy (GC-MS) detected eight known compounds suggesting their possible involvement in the anti-MRSA, anti-adherence, and antioxidant activities. 2. Results 2.1. Phylogenetic Analysis of Strain MUSC 125 The partially complete 16S rRNA gene sequence of strain MUSC 125 strain (GenBank accession number KF682180) was aligned with other strains that appeared to share highly similar 16S rRNA gene sequences from GenBank/EMBL/DDBJ database. Strain MUSC 125 showed the highest percentage of 16S rRNA gene sequence similarities of 99.93% to Streptomyces pluripotens MUSC 135T and followed by Streptomyces cinereospinus (99.24%) and Streptomyces mexicanus (99.17%). The phylogenetic tree constructed showed strain MUSC 125 forming distinct clade with Streptomyces deserti C63T and Streptomyces violascens ISP5183T (Figure1). The culture was deposited in the Marine Culture Collection of China, Third Institute of Oceanography, State Oceanic Administration, Fujian (P.R. China), and the accorded accession number is MCCC 1K03220. Molecules 2020, 25, x FOR PEER REVIEW 4 of 23 Figure 1. Neighbour-joiningFigure 1. Neighbour-joining phylogenetic
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